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Human Remains from the Pleistocene-Holocene Transition of Southwest China Suggest a Complex Evolutionary History for East Asians

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Human Remains from the Pleistocene-Holocene Transition of Southwest China Suggest a Complex Evolutionary History for East Asians Human Remains from the Pleistocene-Holocene Transition of Southwest China Suggest a Complex Evolutionary History for East Asians Darren Curnoe1*, Ji Xueping2,3*, Andy I. R. Herries4, Bai Kanning5, Paul S. C. Tac¸on6, Bao Zhende7, David Fink8, Zhu Yunsheng5, John Hellstrom9, Luo Yun7, Gerasimos Cassis1, Su Bing10, Stephen Wroe1, Hong Shi10, William C. H. Parr1, Huang Shengmin11, Natalie Rogers1 1 School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia, 2 Yunnan Institute of Cultural Relics and Archeology, Kunming, Yunnan, China, 3 Archeology Research Center, Yunnan University, Kunming, Yunnan, China, 4 Archaeomagnetism Laboratory, Archaeology Program, School of Historical and European Studies, La Trobe University, Melbourne, Victoria, Australia, 5 Honghe Prefectural Institute of Cultural Relics, Mengzi, Yunnan, China, 6 Place, Evolution and Rock Art Heritage Unit, School of Humanities, Gold Coast Campus, Griffith University, Southport, Queensland, Australia, 7 Mengzi Institute of Cultural Relics, Mengzi, Yunnan, China, 8 Institute for Environmental Research, Australian Nuclear Science and Technology Organisation, Sydney, Australia, 9 School of Earth Sciences, University of Melbourne, Melbourne, Victoria, Australia, 10 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology and Kunming Primate Research Centre, Chinese Academy of Sciences, Kunming, China, 11 Youjiang Nationalities Museum, Baise, Guangxi, China Abstract Background: Later Pleistocene human evolution in East Asia remains poorly understood owing to a scarcity of well described, reliably classified and accurately dated fossils. Southwest China has been identified from genetic research as a hotspot of human diversity, containing ancient mtDNA and Y-DNA lineages, and has yielded a number of human remains thought to derive from Pleistocene deposits. We have prepared, reconstructed, described and dated a new partial skull from a consolidated sediment block collected in 1979 from the site of Longlin Cave (Guangxi Province). We also undertook new excavations at Maludong (Yunnan Province) to clarify the stratigraphy and dating of a large sample of mostly undescribed human remains from the site. Methodology/Principal Findings: We undertook a detailed comparison of cranial, including a virtual endocast for the Maludong calotte, mandibular and dental remains from these two localities. Both samples probably derive from the same population, exhibiting an unusual mixture of modern human traits, characters probably plesiomorphic for later Homo, and some unusual features. We dated charcoal with AMS radiocarbon dating and speleothem with the Uranium-series technique and the results show both samples to be from the Pleistocene-Holocene transition: ,14.3-11.5 ka. Conclusions/Significance: Our analysis suggests two plausible explanations for the morphology sampled at Longlin Cave and Maludong. First, it may represent a late-surviving archaic population, perhaps paralleling the situation seen in North Africa as indicated by remains from Dar-es-Soltane and Temara, and maybe also in southern China at Zhirendong. Alternatively, East Asia may have been colonised during multiple waves during the Pleistocene, with the Longlin-Maludong morphology possibly reflecting deep population substructure in Africa prior to modern humans dispersing into Eurasia. Citation: Curnoe D, Xueping J, Herries AIR, Kanning B, Tac¸on PSC, et al. (2012) Human Remains from the Pleistocene-Holocene Transition of Southwest China Suggest a Complex Evolutionary History for East Asians. PLoS ONE 7(3): e31918. doi:10.1371/journal.pone.0031918 Editor: David Caramelli, University of Florence, Italy Received December 19, 2011; Accepted January 20, 2012; Published March 14, 2012 Copyright: ß 2012 Curnoe et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was funded by the Australian Research Council. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (DC); [email protected] (JX) Introduction inadequate dating [1,2–3]. For clarity, we consider East Asia to comprise the geographic region bordered by the Ural Mountains Research about the evolution of modern humans has histori- in the west, the Himalayan Plateau in the southwest, Bering Strait cally focused on the fossil records of Europe and Africa as well as in the northeast, and extending into island southeast Asia. the Levantine corridor connecting them. As a result, the role of the One widely discussed candidate for the oldest modern human in vast Asian continent in this evolutionary episode remains largely East Asia is the skeleton from Liujiang, southern China [2]. Yet, unknown. Human remains from the Upper Pleistocene of South the geological age of this individual has ‘‘been an everlasting Asia are scarce, being confined to just two sites possibly within the dispute since the discovery of the fossils in 1958’’ as ‘‘there is no 33-25 thousand years (or ka) range [1]. In East Asia, human fossils documentation on the exact stratigraphic position of the human are more numerous [2], but their significance has been difficult to remains’’ [4, p. 62]. As a result, its estimated age lies within the assess due to poor knowledge of their geological context and broad range of .153-30 ka [2,4]. The age of the Upper Cave PLoS ONE | www.plosone.org 1 March 2012 | Volume 7 | Issue 3 | e31918 Human Remains from Southwest China (Zhoukoudian) remains is similarly problematic and has been a lineages of modern Northeast Asians and Europeans [15]. Several major source of uncertainty since their discovery in the 1930s, with later migrations seem to have occurred within the region, some estimates ranging from ,33-10 ka [2,4]. Furthermore, the Niah associated with the Neolithic [12–14]. Finally, DNA extracted from Cave child from East Malaysia possesses uncertain provenience a .50 ka hominin fossil from Denisova Cave in Central Asia [5]. However, a recent field and lab program aiming to assess the belonging within the Neandertal lineage shares features exclusively stratigraphy and dating of the deposits at the site has proposed an with Aboriginal Southeast Asians and Australasians [16–18]. This age of ,45-39 ka for this cranium [5]. has been interpreted as: 1) evidence for interbreeding between the Most other candidates for the earliest modern humans in East ‘Denisovans’ and the earliest modern humans to colonise the region; Asia are similarly problematic. Among the human remains and 2) implying occupation of Southeast Asia by this archaic recovered from Tabon Cave, Philippines, the only taxonomically population during the Upper Pleistocene [16–17]. diagnostic specimen is a frontal bone assigned to H. sapiens [6], and Given the central importance of the East Asian fossil record to dated to 16.562 ka [7]. Moreover, the oldest specimen from the site testing regional and global scenarios of human evolution, in 2008 – directly dated to 47+11/210 ka [7] – might be from an we began a collaborative research project with the aim of orangutan [6]. At Callao Cave, Luzon, a hominin metatarsal has determining the age and providing detailed comparisons of possible been directly dated to an estimated 66.761 ka [8]. This specimen is, Pleistocene human remains from southwest China. This paper however, difficult to classify reliably, making its assignment to H. focuses on human remains from two localities: Longlin Cave sapiens uncertain [8]. A recently described individual from Tianyuan (Longlin or LL) and Malu Cave (Maludong or MLDG) (Figure 1). Cave near Zhoukoudian town, northeast China, is estimated to be The Longlin human remains were discovered opportunistically in ,42-39 ka [9]. The Tianyuan partial skeleton comprises 34 pieces 1979 by a petroleum geologist (Li Changqing) in a cave near De’e, apparently from the same individual, its femur being directly dated Longlin County, Guangxi Zhuang Autonomous Region, Guangxi to 40,3286816 cal. yr BP [9]. This specimen seems to provide the Province (Figure 1). A block of consolidated fine-grained sediment best candidate for the earliest modern human in East Asia, but is containing the human remains, unidentifiable animal bones, charcoal significantly younger (.20 kya) than genetic clock estimates for and burnt clay fragments was removed from the cave and taken to colonisation of the region (see below). Finally, a mandibular Kunming in neighbouring Yunnan Province shortly after its fragment from Zhirendong, southern China, has been dated on discovery. A partial mandible and some fragments of postcranial stratigraphic grounds to .100 ka [10]. Unfortunately, the specimen bone were prepared from the block at this time [2], although, the is fragmentary and possesses a mosaic of archaic and modern remainder of the skull and other postcranial bones were only characters also making its taxonomic status unclear [10–11]. prepared from the sediment by our team during 2010. During Given ongoing uncertainty surrounding the human fossil record, preparation we recovered a thin flowstone adhering to the surface of palaeoanthropologists have come to rely on the results of genetic the
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